A threshold mechanism mediates p53 cell fate decision between growth arrest and apoptosis

Cell Death Differ. 2013 Apr;20(4):576-88. doi: 10.1038/cdd.2012.155. Epub 2013 Jan 11.

Abstract

The p53 tumor suppressor responds to certain cellular stresses by inducing transcriptional programs that can lead to growth arrest or apoptosis. However, the molecular mechanisms responsible for choosing between these two cell fates are not well understood. Previous studies have suggested that p53 selectively activates proarrest target genes, due to the higher affinity of p53 for their promoters compared with proapoptotic genes. Here we show using microarray and chromatin immunoprecipitation that p53 binds to and transcriptionally activates both its proarrest and proapoptotic target genes proportionally to induced p53 expression levels. Further, we provide evidence that to trigger apoptosis, cells must overcome an apoptotic threshold, whose height is determined by expression levels of p53 and its targets, the duration of their expression and the cellular context. We demonstrate in multiple cells lines that below this threshold, expression levels of p53 and its targets were sufficient to induce arrest but not apoptosis. Above this threshold, p53 and its targets triggered extensive apoptosis. Moreover, lowering this threshold with inhibitors of antiapoptotic Bcl-2 family proteins sensitized cells to p53-induced apoptosis. These findings argue that agents that lower the apoptotic threshold should increase the efficacy of p53-mediated cancer therapy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Antibiotics, Antineoplastic / pharmacology
  • Apoptosis* / drug effects
  • Cell Line
  • Down-Regulation
  • Doxorubicin / pharmacology
  • Doxycycline / pharmacology
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • G1 Phase Cell Cycle Checkpoints / drug effects
  • Humans
  • Imidazoles / pharmacology
  • Piperazines / pharmacology
  • Promoter Regions, Genetic
  • Protein Binding
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Transcriptional Activation
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism*
  • Up-Regulation

Substances

  • Antibiotics, Antineoplastic
  • Imidazoles
  • Piperazines
  • Proto-Oncogene Proteins c-bcl-2
  • Tumor Suppressor Protein p53
  • nutlin 3
  • Doxorubicin
  • Doxycycline